review article The genetic legacy of the Quaternary ice ages Godfrey Hewitt School of Biological Sciences, University of East Anglia, Norwich NR4 7TJ, UK ............................................................................................................................................................................................................................................................................ Global climate has fluctuated greatly during the past three million years, leading to the recent major ice ages. An inescapable consequence for most living organisms is great changes in their distribution, which are expressed differently in boreal, temperate and tropical zones. Such range changes can be expected to have genetic consequences, and the advent of DNA technology provides most suitable markers to examine these. Several good data sets are now available, which provide tests of expectations, insights into species colonization and unexpected genetic subdivision and mixture of species. The genetic structure of human populations may be viewed in the same context. The present genetic structure of populations, species and communities has been mainly formed by Quaternary ice ages, and genetic, fossil and physical data combined can greatly help our understanding of how organisms were so affected. The study of palaeoclimates is a particularly active research field that These severe climatic oscillations produced great changes in species is producing much data and increasingly coherent explanations. distributions, and these have been described in some detail, particularly The Earth’s climate became cooler through the Tertiary (65 million from the fossil records of pollen and beetles in Europe and North years (Myr)) with frequent oscillations that increased in amplitude America1,9. Species went extinct over large parts of their range, some and lead to the series of major ice ages of the Quaternary (2.4 Myr to dispersed to new locations, some survived in refugia and then the present). The evidence for such global fluctuations in climate expanded again, and this must have occurred repeatedly. comes particularly from cores of the sea bed, lake bottoms and ice During major glaciations the polar ice sheets spread considerably, sheets, which are analysed for carbon and oxygen isotopes, radi- and temperature, marine and vegetation zones were compressed olarian species, pollen types and other biological and physical towards the Equator2. Mountain blocks like the Alps, Andes, signatures1,2. Rockies and Yakutsk ranges also had considerable glaciation, so that the large volume of accumulated ice reduced sea levels by about Ice ages and species distributions 120 m (ref. 10). This produced land bridges in several parts of the While the Antarctic ice cap grew from the Oligocene (35 Myr), the world (Fig. 1). In warmer parts species descended from mountains. Arctic ice cap became established about 2.4 Myr ago, the beginning Tropical rainforest was restricted and dissected, and there was of the Quaternary. From then until 0.9 Myr ago, the ice sheets extension of deserts and savannah11. It is apparent that these advanced and receded with a roughly 41,000-yr (41-kyr) cycle; major climatic shifts were felt differently across the globe owing thereafter they have followed a 100-kyr cycle and become increas- to regional differences in landform, ocean currents and latitude. ingly dramatic. Such periodicity suggests a controlling mechanism, Furthermore, species responded individually, and their range and the Croll–Milankovitch theory proposes that the regular changes were particular to local geography and climate. variations in the Earth’s orbit around the Sun are the pacemakers of the ice-age cycles1,2. The main orbital eccentricity has a 100-kyr Genetic consequences cycle, variation in the Earth’s axial tilt has a 41-kyr cycle, and In Europe and North America, an extensive network of pollen cores precession due to the Earth’s axial wobble has a 19–23-kyr cycle; tells us that species now inhabiting boreal and temperate regions these all modify the insolation of the Earth and the energy it had their ice-age refugia south of the ice and permafrost. Post- receives. Much energy is transported by the oceanic circulation glacial expansion into new territory was previously suggested to be system, and the interaction of orbital variation and currents leads to important in the geographic distribution of population and species significant climate changes2,3. genomes12. It was remarkably rapid for many species, and the It is now possible to extract ice cores of ,2 km in length and analyse suddenness of the large climatic shifts recorded in the recent ice the annually layered snow for entrapped gases, isotopes, acidity, dust cores helps explain this. Populations at the northern limits of the and pollen. Some recent cores sample ice over 400 kyr (ref. 4), but most refugial range would have expanded into often large areas of suitable go back ,125 kyr from the present to the previous (Eemian) inter- territory. This leading edge expansion would probably be by long- glacial. Long pollen cores stretching back to 400 kyr are also becoming distance dispersers that set up colonies and rapidly expanded to fill available5. Along with other measures, these are providing a detailed the area before others arrived. This would be repeated many times picture of the last glacial cycle and glimpses of the preceding ones over a long colonizing route, and these founding events would lead (Fig. 1). The Greenland (Arctic) and Vostok (Antarctic) ice cores are to loss of alleles and homozygosity13. Modelling and simulations of particularly informative, offering fine temporal resolution and such range expansion show that leptokurtic dispersal produces large continuity2. This has revealed surprising oscillations of climate on areas of homozygosity as compared with normal or stepping-stone a millennial scale within the main 100-kyr cycle. The Greenland Ice modes, and these homogeneous areas persist in space and increase Core Project (GRIP) identifies some 24 interstadials through the last with time14. Secondary oscillations within the main expansion ice age with average temperature rising rapidly by ,7 8C over just increase the effect. Rapid colonization by this leading edge model decades. Further ice and sediment cores from around the world are in any part of the world should produce areas with reduced genomic demonstrating the global scale of these major climatic events6,7.As variability. more long cores of ice, sediment and pollen become available, it will Where the postglacially colonized regions are known from the be possible to produce a synthesis of the effects of these rapid fossil record (in Europe and North America), a growing number of climatic switches on plant and animal life worldwide5,8. studies show them to have lower genetic diversity15, and a fine NATURE | VOL 405 | 22 JUNE 2000 | www.nature.com © 2000 Macmillan Magazines Ltd 907 review article analysis of 41 North American fish species demonstrates this genome structure could diverge considerably. clearly16. These studies also reveal that equivalent genomes occupy The rapid expansion across large parts of Europe and North larger ranges in these colonized areas, as produced in simulation America was not followed by all species, and was probably much modelling14. slower in some other regions, particularly the tropics. This would An interesting corollary of this leading edge expansion is that maintain a larger effective population size and retain much more when populations have filled the space it is much more difficult for genetic diversity. Various parts of the same species range may have those behind them to advance, because they must disperse and been colonized at different rates owing to physical barriers or prior reproduce logistically, and not exponentially like the original inhabitants, producing distinct genetic structures. Mountain blocks scattered colonists13. This high-density barrier will mean that in southern temperate regions and the tropics would allow slower boundaries between expanded edge and blocked interior genomes altitudinal shifts in range, tending to retain allelic diversity. Their will tend to persist for some time and be seen in present surveys15,16. varied topography also tends to subdivide the species into popula- It is also likely that during a range change a retreating rear edge will tions that may evolve independently with only occasional gene flow, suffer shrinkage, dissection and extinction, so that the last surviving perhaps only every glaciation or interstadial. It would seem that the population should be severely bottlenecked. This could be in the interpretation of present genetic structure needs to consider such vanguard of the recolonization. interaction of biology, geography and climatic shifts. With expansion of range there will also be selection and adapta- tion to different environments and new neighbours13,15. For exam- Suitable DNA markers ple, the reproductive biology of many plants is suited to different Modern DNA technology allows genetic diversity to be measured as light and temperature regimes across their present range from south single-base changes in many individuals, and a variety of sequences to north17, which has been produced with postglacial colonization. have been used (Table 1). As the Quaternary is 2.4 Myr old, most The same is true of insects, and particularly nice demonstrations are DNA sequences will diverge little over the ice ages, and few new seen